17Ann. appl. Biol. (2004), 145:17-24Printed in UK

*Author E-mail: nigel.halford@bbsrc.ac.uk

© 2004 Association of Applied Biologists

Prospects for genetically modified crops

By NIGEL G HALFORD*

Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire,AL5 2JQ, UK

(Accepted 4 May 2004; Received 20 February 2004)

Summary

Genetically modified (GM) crops have been in use commercially around the world for almost adecade. This review covers the successes and failures of GM crop varieties in that time, the currentstatus of GM crop adoption and the traits that are being used. It also describes some of the GM cropsthat might come on to the market in the next decade. The barriers in the way of GM crop developmentin Europe, including consumer hostility, the difficulty in gaining official approval and discriminatorylabelling laws are discussed.

Key words: GM crop status, GM crop traits, future applications of GM crops, farm scale evaluations,GM food legislation and labelling

Introduction

Genetic modification using transgenesis is nowan established technique in plant breeding. That isnot to say that it is sweeping away every othertechnique, rather that it is an additional tool in theplant breeder�s toolbox. All plant breeding, ofcourse, involves the alteration (or, if you like,modification) of plant genes, whether it is throughthe crossing of different varieties, the introductionof a novel gene into the gene pool of a crop species,perhaps from a wild relative, or the artificialinduction of random mutations in the DNA of a cropplant through chemical or radiation mutagenesis.Recently, however, the term genetic modification hasbeen applied to the technique of inserting a singlegene or small group of genes into the DNA of anorganism artificially.

The methods available for the genetic modificationof plants are described in detail elsewhere (e.g.Halford, 2003; Slater et al., 2003) and I will notdescribe them here. The technique has becomeestablished in plant breeding because it has someadvantages over other techniques. These advantagesare:• It allows genes to be introduced into a crop plantfrom any source (although it is likely that the use ofanimal genes would not be acceptable to consumers,at least in food crops).• It is relatively precise, single genes can betransferred (this is not possible in conventionalbreeding).• Genes and their products can be tested extensivelyin isolation before use to ensure their safety.• Genes can be �cut and pasted� in the laboratory to

change when and where in a plant they are active,and to change the properties of the proteins that theyproduce.

There is also, however, a significant down-sidefor the plant breeder in using genetic modificationto produce new varieties for the European market.This is that any genetically modified (GM) crop orfood derived from it has to be approved for usewithin the European Union, and approval isextremely difficult to obtain. Furthermore, any foodcontaining GM crop material above a threshold of0.9% has to be labelled, while novel foods producedin any other way do not. This is preventing thedevelopment of new GM traits specifically for theEuropean market. Nevertheless, the use of GM cropsaround the world continues to increase.

Current Status of GM Crops

Detailed information on the uptake of GM cropsby farmers around the world has been provided forseveral years by Clive James at the InternationalService for the Acquisition of Agri-biotechApplications (ISAAA) (www.isaaa.org). In 2003,the ISAAA reported that GM crops were beinggrown commercially in 18 countries: Argentina,Brazil, Canada, Colombia, Honduras, Mexico,Uruguay and the USA in the Americas; Bulgaria,Germany, Romania and Spain in Europe; China,India, Indonesia and the Philippines in Asia;Australia and South Africa. Of these, Argentina,Brazil, Canada, China and the USA dominate interms of total area. The global area of land plantedto GM crops in 2003 was approximately 65 millionha, an increase of 15% on 2002.

18 NIGEL G HALFORD

More than half of this area is accounted for byherbicide-tolerant GM soybean, in fact more thanhalf of the global soybean crop is now GM. Theother major GM crops are maize (corn), cotton andoilseed rape (canola). There are also relatively smallareas planted to GM virus-resistant papaya andsquash and slow-ripening tomatoes.

GM Traits Being Used Successfully inCommercial Agriculture

The most successful traits to date (and it is difficultseeing them being overtaken) are those aimed at thefarmer: herbicide tolerance (soybean, oilseed rape,cotton and maize) and insect resistance (cotton andmaize). Traits affecting the quality or the nutritionalvalue of the product have been more difficult todevelop and market, but there are signs that thesesorts of crops will become important in developingcountries. It is fair to say, at present, that the numberof traits that have been commercialised successfullyis small.

Herbicide toleranceHerbicides have been used since the 1950s, long

before the advent of genetic modification, and arean essential part of weed control for farmers indeveloped countries. Most herbicides are selectivein the types of plant that they kill and a farmer hasto select a herbicide or combination of herbicides,applied at different times in the season, that istolerated by the crop that he is growing but kills theproblem weeds. Some of these herbicides have togo into the ground before planting, some pose ahealth risk to farm workers and some are persistentin the soil, making crop rotation difficult. They allrequire equipment and labour to apply and they allcost money.

Herbicide-tolerant GM crops were produced toovercome or reduce these problems. The first to begrown commercially were soybeans developed byMonsanto that were modified to tolerate the broad-range herbicide, glyphosate (Padgette et al., 1995).Glyphosate is relatively safe to use, does not persistlong in the soil because it is broken down by micro-organisms and is taken up through the foliage of aplant, so it is effective after weeds have becomeestablished. It is also relatively cheap. Its target is5-enolpyruvoylshikimate 3-phosphate synthase(EPSPS), an enzyme in the shikimate pathway thatis required for the synthesis of many aromatic plantmetabolites, including some amino acids. Theshikimate pathway is not present in animals, henceglyphosate�s low toxicity to animals. The gene thatconfers tolerance of the herbicide is from the soilbacterium Agrobacterium tumefaciens and makes anEPSPS that is not affected by glyphosate.

Over 150 US seed companies now offer varieties

carrying the trait and 81% of the US soybean cropin 2003 was glyphosate-tolerant (Benbrook, 2003).This success is due to simple factors: simplified andsafer weed control, reduced costs and moreflexibility in crop rotation. Overall, between 1995and 1998 there was estimated to be a reduction of$380 million in annual herbicide expenditure by USsoybean growers (Gianessi et al., 2002). However,farmers who used glyphosate-tolerant varieties hadto pay a technology fee of $6 per acre. This reducedthe overall cost saving to $220 million. Anotherreport has suggested that although herbicide use fellwith the introduction of these crops it has since risen(Benbrook, 2003). The fact that the GM system hasled to a switch to conservation tillage systems whichinvolve leaving weeds and stubble undisturbed overwinter and then spraying with herbicide in the springcould explain an increase in herbicide use. If this isthe case the consequent benefits of reductions in soilerosion and pollution from run-off would faroutweigh the disadvantage of a modest increase inherbicide use. Nevertheless, it is not clear how thesereports should reach such different conclusions.

There are two other broad-range herbicide tolerantGM systems in use, involving the herbicidesgluphosinate (or glufosinate) and bromoxynil, bothmarketed by Bayer. The gene used to make plantsresistant to gluphosinate comes from the bacteriumStreptomyces hygroscopicus and encodes an enzymecalled phosphinothricine acetyl transferase (PAT).This enzyme detoxifies gluphosinate. Crop varietiescarrying this trait include varieties of oilseed rape,maize, soybeans, sugar beet, fodder beet, cotton andrice. The oilseed rape variety has been particularlysuccessful in Canada. Bromoxynil tolerance isconferred by a gene isolated from the bacteriumKlebsiella pneumoniae ozanae. This gene encodesan enzyme called nitrilase, which convertsbromoxynil into a non-toxic compound. So far thishas only been used commercially in Canadianoilseed rape.

Interestingly there is a fourth broad-rangeherbicide-tolerance trait available in commercialoilseed rape varieties in Canada. The herbicide inthis case is imidazolinone and the varieties wereproduced by Pioneer Hi-Bred, now part of DuPont.However, the trait was produced by mutagenesis,not genetic modification.

Herbicide tolerance has now been engineered intomany crop species and is undoubtedly the mostsuccessful GM trait to be used so far. In the USA in2003, 59% of the upland cotton and 15% of the maizewas herbicide-tolerant (Benbrook, 2003), as well asthe 81% of the soybean crop already discussed.Herbicide-tolerant soybeans have been adopted evenmore enthusiastically in Argentina and now accountfor 95% of the market, while herbicide-tolerantoilseed rape has taken 66% of the market in Canada.

19Prospects for genetically modified crops

is to use antisense or co-suppression techniques(Grierson et al., 1996) to block the activity of viralgenes when the virus infects a plant. A potato varietycarrying a replicase gene from potato leaf roll virus(PLRV) was marketed by Monsanto in the 1990s,later in combination with the Bt insect-resistancetrait. These GM potato varieties have since beenwithdrawn in the USA because of reluctance to usethem in the important fast-food industry.

This technology is being applied to many otherplant virus diseases, just one example of resistancebeing achieved at least under trial conditions beingwith potato tuber necrotic ringspot disease (Racmanet al., 2001). It has tremendous potential fordeveloping countries where losses to viral diseasesare the greatest and have the most severeconsequences.

Modified oilsOilseed rape was first grown in the UK during the

second world war to provide industrial oil, high inerucic acid (which is poisonous to humans), andthese varieties are still grown today for that purpose.In the second half of the last century, however,varieties were bred with reduced levels of erucic acidand another group of poisonous compounds calledglucosinolates. When these varieties were passedas acceptable for human consumption (oilseed rapereceived its seal of approval from the Food and DrugAdministration of the USA in 1985), Canadianproducers came up with the name Canola for edibleoilseed rape oil. This name was adopted all overNorth America as the name not only for the edibleoil but also for the crop itself.

A problem for farmers who grow oilseed rape isthat its oil is one of the cheapest edible oils on themarket. The value of the crop is, therefore, relativelylow and there is a lot of interest in increasing it.This has been achieved through genetic modificationby introducing a gene from the California Bay plantthat causes an accumulation of lauric acid toapproximately 40% of the total oil content, comparedwith 0.1% in unmodified oilseed rape. Lauric acidis a detergent traditionally derived from coconut orpalm oil.

A different modification has been made to the oilof soybean. In this case, the genetically modifiedvariety accumulates oleic acid to approximately 80%of its total oil content, compared with approximately20% in non-GM varieties (Mazur et al., 1999;Kinney, 1996). This was achieved by co-suppression(Grierson et al., 1996) of a gene that encodes anenzyme that converts oleic acid to linoleic acid.Oleic acid is very stable at high temperatures and atpresent the oil from the GM soybeans is used forindustrial purposes.

Relatively small amounts of these GM oilseed rapeand soybean varieties are grown to contract, but

Insect resistanceOrganic and salad farmers have been using a

pesticide based on a soil bacterium, Bacillusthuringiensis (Bt), for several decades. Thebacterium produces a protein called the Cry proteinthat is toxic to some insects but has no toxicity tomammals, birds or fish. Different strains of thebacterium produce different versions of the proteinthat are effective against different types of insects.Cry1 proteins, for example, are effective against thelarvae of butterflies and moths, while Cry3 proteinsare effective against beetles.

The Cry1A gene has now been introduced intoseveral crop species (de Maagd et al., 1999) and themodified varieties are generally referred to as Btvarieties. As with herbicide tolerance, the benefitsof using the insect-resistant GM crops depend onmany factors, most obviously the nature of the majorinsect pests in the area (not all are controlled by Bt)and the insect pressure in a given season. However,Bt varieties have been successful in many parts ofthe USA (in 2003, 29% of the maize and 41% of theupland cotton crop was Bt) and Bt cotton in particularis gaining ground in Australia, China, India and thePhilippines. Farmers who use Bt varieties citereduced insecticide use and/or increased yields asthe major benefits. A further, unexpected benefit ofBt maize varieties is that the Bt grain contains loweramounts of fungal toxins (mycotoxins) such asaflatoxin and fumicosin.

A different Cry gene, Cry3A, has been used tomodify potato to make it resistant to the Coloradobeetle. These GM potato varieties were withdrawnin the USA due to poor sales, farmers preferring touse broad-range insecticides instead. However, theymay have a role to play elsewhere in the world wherethe Colorado beetle is a problem.

Virus resistanceThere are two methods currently in use to

genetically modify plants to be resistant to viruses.The first arose from studies into the phenomenon ofcross protection, in which infection by a mild strainof a virus induces resistance to subsequent infectionby a more virulent strain (reviewed by Culver, 2002).Modifying a plant with a gene that encodes the viralcoat protein has been found to mimic thephenomenon.

An example of the commercialisation of thistechnology comes from the papaya industry in thePuna district of Hawaii (Ferreira et al., 2002;Gonsalves, 1998). After an epidemic of papayaringspot virus (PRSV) in the 1990s almost destroyedthe industry growers switched to a virus-resistantGM variety containing a gene that encodes a PRSVcoat protein. The GM variety was successful andprobably saved the papaya industry in Hawaii.

The other method used to engineer virus resistance

20 NIGEL G HALFORD

those farmers who can get in on this business benefitfrom a premium price for their crop.

Slow-ripening fruit Fruit ripening is a complex process that brings

about the softening of cell walls, sweetening andthe production of compounds that impart colour,flavour and aroma. The process is induced by theproduction of a plant hormone, ethylene. Theproblem for growers and retailers is that ripening isfollowed sometimes quite rapidly by deteriorationand decay. Genetic modification has been used toslow ripening down or to lengthen the shelf-life ofripe fruit by interfering either with ethyleneproduction or with the processes that respond toethylene. This technology has the potential not onlyto improve the produce of western farmers but alsoto enable farmers in tropical countries to sell fruit tocustomers in Europe and North America. So far,however, the only examples of its commercial useare in tomato.

The first GM tomatoes with increased shelf lifehad reduced activity of an enzyme calledpolygalacturonase (PG), which contributes to cellwall softening. A fresh fruit GM tomato, Flavr Savr,with this trait was marketed by Calgene in the mid-1990s but did not prove popular with consumers.Zeneca introduced the trait into tomatoes used forprocessing. The GM tomatoes have a higher solidcontent than conventional varieties, reducing wasteand processing costs in paste production and givinga paste of thicker consistency. This product provedvery popular in the UK from its introduction in 1996until 1999 when retailers withdrew it in response toanti-GM hostility.

Some GM tomato varieties with delayed ripeningare still on the market in the USA. They havereduced activity of the enzyme aminocyclopropane-1-carboxylic acid (ACC) synthase, which is requiredfor ethylene synthesis. ACC has also been targetedby Monsanto using a gene from a bacterium,Pseudomonas chlororaphis, that encodes an enzymecalled ACC deaminase, which breaks down ACC.A similar strategy has been adopted by Agritope,Inc., to break down another of the precursors ofethylene, S-adenosyl methionine (SAM), using agene encoding an enzyme called SAM hydrolase.These products are not yet on the market butdemonstrate that there is still considerable interestin modifying fruit ripening and shelf-life.

The StarLink Incident

Not everything has run smoothly in thecommercial application of GM crops. The mostcostly mistake involved several Bt maize varietiesproduced by Aventis (now part of Bayer) andmarketed in the USA under the trade name StarLink.

StarLink contained a different version of the Crygene to that in other Bt varieties on the market(Cry9C instead of Cry1A) and was also tolerant ofthe herbicide gluphosinate. StarLink was notapproved for human consumption but, inexplicablygiven that maize is an outbreeding crop, theEnvironmental Protection Agency approvedStarLink for commercial growing as an animal feedin 1998. Inevitably, cross-pollination occurredbetween StarLink and maize varieties destined forhuman consumption and StarLink had to bewithdrawn. Aventis agreed to buy back the entireStarLink crop of 2000 at a premium price.

Future Applications in GM Crops

Production of industrial oils and pharmaceuticalfatty acids

Two examples of GM crops with modified oilcontent are described above but they are undoubtedlyonly the first of many. One application of thistechnology is in the production of oils withnutritional or pharmaceutical properties. Several oilsproduced by plants have pharmaceutical properties,including gamma-linolenic acid (GLA), which isfound in borage and evening primrose, andarachidonic acid (AA) which is only found in a fewmosses and fungi. GLA is used in the treatment ofskin conditions such as atopic eczema and also hasanti-viral and anti-cancer properties. AA is aconstituent of breast milk and is important for brainand eye development in infants. The aim ofbiotechnologists is to take the genes that encode theenzymes responsible for making these fatty acidsand engineer them into crop plants and there arealready examples of this being done successfully(reviewed by Napier et al., 1999; Napier &Michaelson, 2001).

Nutritional valueConsumers in the developed world who take

advantage of the world�s harvest of fresh fruit,vegetables, bread, meat and dairy products that isavailable to them all year round probably have littleneed for an increase in the nutritional value of theirfood. Many, however, do not, and there is anargument for increasing the nutritional value of foodsthat consumers like rather than persuadingconsumers to change their diets. Nutritional valueis also a selling point with some foods, breakfastcereals being a good example. Examples of the manypotential targets for plant breeders andbiotechnologists are folic acid, deficiency of whichmay cause gastrointestinal disorders, anaemia andbirth defects, and the fat-soluble vitamins E and K,deficiencies in which are associated with arterialdisease and, in the case of vitamin K, post-menopausal osteoporosis. Strategies for increasing

21Prospects for genetically modified crops

the levels of some of these nutrients are describedby Herbers (2003). The real need for nutritionalenhancement of foods, however, is in developingcountries, where a limited amount and range offoodstuffs may be available or affordable.

An example of a severe but avoidable healthproblem in poor countries is night and total blindnessbrought about by vitamin A deficiency. This isassociated in particular with a reliance on rice as astaple food and it is estimated that a quarter of amillion children go blind each year because ofvitamin A deficiency in South East Asia alone.

There are many ways to tackle this problem andmany have been tried but so far all have failed. Onepossible solution might be to address the low levelsof vitamin A in rice (rice grain does contain vitaminA but only in the husk, which is discarded becauseit rapidly goes rancid during storage, especially intropical countries). This has been achieved in anexperimental GM rice line called Golden Rice (thename deriving from the colour of the grain) (Ye etal., 2000). Golden Rice actually accumulates β-carotene (a precursor that humans can process intovitamin A) in its seed endosperm. The modificationrequired the introduction of three genes, phytoenesynthase (psy) and lycopene β-cyclase genes fromdaffodil (Narcissus pseudonarcissus), and aphytoene desaturase (crtI) gene from the bacteriumErwinia uredovora. The enzymes encoded by thesegenes convert the compound geranylgeranyldiphosphate, which is present in rice endosperm, intoβ-carotene. This line was then crossed with anotherGM rice line which had been modified with a geneencoding phytase, an enzyme which breaks downphytate, a compound that prevents iron absorption,to make Golden Rice.

Golden Rice is not a commercial variety but thetrait is being crossed into commercial breeding linesat the Rice Research Institute in the Philippines andby plant breeders in India. Even if these programmesare successful, it will still be several years beforecommercial varieties carrying the trait becomeavailable. Nevertheless, the potential of the work isextremely exciting.

Another target of great potential is improving theprotein content of crops in terms of amount andquality. One example where this has been achievedis in potato at the National Centre for Plant GenomeResearch in Delhi. Tuber yield and protein contenthave been increased by introducing the Amaranthushypochondriacus AmMA1 gene, which encodes aseed protein that is rich in essential amino acids(Chakraborty et al., 2000). Potato is not a majorcrop in India, but the same gene is also beingintroduced into rice, sweet potato and cassava.

Improving nutritional value, particularly proteincontent and protein quality, is also relevant to theproduction of animal feed. However, although some

GM crops, for example soybean, maize, cotton andoilseed rape, are used for animal feed, there iscurrently no commercial use of a GM crop that hasbeen modified specifically to improve its nutritionalvalue to animals.

Resistance to fungal diseasesFungal diseases of plants cause severe losses in

crop production and an example of geneticmodification being used to tackle the problem is inthe engineering of potato to make it resistant to lateblight (Song et al., 2003). Late blight is infamousas the cause of the Irish potato famine of the 19th

century and still causes serious crop losses aroundthe world today. The gene that was introduced intothe potato line was called RB and came from a wildMexican potato species called Solanumbulbocastanum.

Salt toleranceMillions of acres of otherwise fertile land in

developed and developing countries are rendereduseless by salt build-up, usually as a result ofirrigation. A possible solution to this problem hasbeen developed using genetic modification toincrease the rate at which a plant cell can removesalt from its cytoplasm and dump it in its vacuole.This involved the over-expression of a gene thatencodes a vacuolar Na+/H+ antiport pump (Apse &Blumwald, 2002). Tomato plants modified in thisway can tolerate salt concentrations several timeshigher than non-GM plants and should survivecomfortably in the salt concentrations of soils thatare currently considered unusable. Salt accumulatesin the leaves but the fruit remains edible and notsalty at all. This means that removal and disposalof the leaf material after harvest actually cleans upthe soil and a few harvests of the GM plants shouldreturn the soil to salt concentrations suitable forgrowth of other crops. Similar technologies arebeing developed to address the problem ofcontamination of soils with heavy metals.

Other traitsThe above is not meant to be a comprehensive

list. Other traits that might be developedcommercially in the future include the ability tosurvive difficult climatic conditions (Araus et al.,2003), improved photosynthetic efficiency (Parry etal., 2003), the synthesis of non-food products suchas pharmaceuticals, including vaccines (Mor et al.,1998), the synthesis of fragrances, pigments andindustrial starch (Burrell, 2003), the removal ofallergens (Tada et al., 1996) and the modification ofmetabolism (Halford et al., 2003; Halford & Paul,2003). Whether or not these advances are made willdepend to some extent on the barriers that are put inthe way of the development of the technology.

22 NIGEL G HALFORD

Barriers to the Development of PlantBiotechnology

Resistance to the use of GM crops is mostsignificant in Europe. A major barrier is consumerhostility, driven in part by an intense anti-GMcampaign waged by pressure groups. The UKgovernment ran a public consultation exercise in2003 called the �GM Nation� debate. This consistedof public meetings organised around the country afterwhich participants were invited to completequestionnaires. Entirely predictably these debateswere dominated by the representatives of pressuregroups and the result was an overwhelming rejectionof GM crops and food. Real consumer attitudes aremuch more complex and difficult to gauge. A pollundertaken by the Institute of Grocery Distributionin August 2003 in the UK found that 47% ofrespondents were not interested in the ingredientsin their food at all. Another 27% would prefer notto eat GM products but would not trouble to look ata label to avoid them, while 13% were happy to eatGM products but another 13% would actively avoidthem. Clearly this is not a simple issue for retailers.

The second barrier in Europe is one of legislationand official approval. This arose at first as an attemptto err on the side of caution as the new technologywas introduced, but it is now clearly a political issue.If a GM crop is to be grown commercially in the EUit must first be granted a Part C consent by theEuropean Commission. An application for consentis submitted to one of the 15 Member States, whichbecomes the lead Competent Authority (CA) for theapplication. If the United Kingdom is the CA for anapplication the dossier, which includes the resultsof safety testing and environmental risk assessment,is reviewed by the Joint Regulatory Authority,comprising the Department for the Environment,Food and Rural Affairs (DEFRA), the ScottishExecutive, the National Assembly for Wales and theDepartment for the Environment in Northern Ireland.Advice is taken from the Advisory Committee onReleases into the Environment (ACRE), theAdvisory Committee on Novel Foods and Processes(ACNFP) and the Advisory Committee on AnimalFeeding-stuffs (ACAF). The CA returns theapplication to the European Commission with anaccept or reject recommendation.

If acceptance has been recommended, a dossier iscirculated to the other Member States, who have 60days to make comment. If they all approve themarketing application the lead CA issues a Part Cmarketing consent, which applies across all MemberStates. In reality, one or more Member States objectsto every application and the Commission passes thedossier to its own Scientific Committee on Plants(SCP), which considers exactly the same questionsalready considered by ACRE. The SCP can consult

two other committees, the Scientific Committee onAnimal Nutrition (SCAN) and the ScientificCommittee on Food (SCF), the equivalents of ACAFand ACNFP.

If the SCP recommends that approval be granted,the Commission asks the Members States to voteagain, this time by the Qualified Majority Voting(QMV) procedure. If there is a QMV in favour thelead Member State should issue consent. But since1998, France, Italy, Denmark, Greece, Austria andLuxembourg have blocked every application. TheCommission then has the option of referring theapplication to the Council of Ministers, who canreject the decision of the Commission but only by aunanimous vote. If this does not happen theCommission should instruct the lead CA to grantconsent. The Commission has been reluctant to usethis option but appears to have become moreassertive on the issue and has exercised it this year(2004) in the case of a Syngenta sweetcorn variety.However this variety is intended for import, not forcultivation in Europe. Three other products, a varietyof Bt maize, glyphosate-tolerant soybean and tomatopaste from GM tomatoes, have had such approvalfor many years.

Any food containing material from GM crops andsold in the EU must be labelled. Up to April 2004vegetable oils, sugar and other refined products thatdo not contain DNA or protein are exempt from thisrule, as are foods that contain small amounts (below1%) of GM material as a result of accidental mixingand food sold in restaurants and other catering outlets(the UK government waived this exemption). InApril 2004 the exemption for refined products willbe dropped (although there are fears that this willlead to fraud since there is no way of policing it),the tolerance level for accidental mixing will bereduced to 0.9% and the law will be extended toanimal feed.

The clear labelling of foods is entirely laudable,but the policy applies solely to GM crop products,not to new crop varieties produced by other methodsor to the products of GM micro-organismscommonly used in yoghurts, cheeses and otherfoodstuffs. The policy could, therefore, be regardedas illogical and discriminatory. Nevertheless, thelack of a clear labelling policy when GM cropproducts first went on sale in Europe is one of thefactors that led to consumer hostility.

The UK Farm-Scale Evaluations (FSE)Programme

In 2000 the UK government erected another barrierto the commercial use of GM crops. At that time agluphosinate-tolerant maize variety, Chardon LLfrom Bayer, had been granted Part C consent andgluphosinate-tolerant oilseed rape and glyphosate-

23Prospects for genetically modified crops

tolerant sugar beet were expected to be grantedconsent shortly after. The government negotiated avoluntary agreement with the companies involvedthat these varieties would not be marketed until a 3-yr programme of farm-scale evaluations had beencarried out to compare the environmental effects ofthe GM crop and its non-GM equivalent togetherwith the appropriate herbicide regime. The resultsof these studies were published in a special editionof the Philosophical Transactions: BiologicalSciences of the Royal Society (Vol. 358, No. 1439,29 November 2003).

These studies produced a huge amount of data andit is not possible to review it all here. In briefsummary, it was found that for the sugar beet andoilseed rape varieties the numbers of weeds andconsequently insects in the GM crop were lower thanin the non-GM equivalent. This was widely reportedas showing that GM crops were �bad for theenvironment�. In reality it meant that the herbicideregime used with the GM varieties did what it wassupposed to do. The possible advantages to thefarmer of growing herbicide-tolerant GM crops (forexample May (2003) estimated that sugar beetfarmers could save £150 ha-1 yr-1) were notconsidered and different ways of using the crops andthe herbicide were not included in the study. As aresult, the Government has put off approval of thesevarieties until the companies involved, Monsantoand Bayer, can show that they can be used in an�environmentally-friendly� manner. It is not clearwhether Monsanto and Bayer are interested in doingthis.

Both GM and non-GM maize were found toharbour fewer weeds and insects than the other cropsstudied (maize is taller and weed growth is restrictedby shading). However, the GM variety was �better�than the non-GM variety. In fact this relatively poorweed control was a concern to at least one farmerparticipating in the study (personal communication).However, the herbicide used on the non-GM maizein the study and used by most maize farmers in theUK was atrazine, which has just been banned foruse within the EU because of its toxicity. The GMmaize/gluphosinate combination represented apossible alternative.

In March 2004 the UK Government announcedthat it agreed in principle to the commercialcultivation of Chardon LL maize but that a numberof constraints would be placed on its use. In April2004 Bayer announced that, in view of the fact thatdetails of these constraints had still not been madeavailable, resulting in another period of delay, andthat the variety was already 5 years old, it was notworth proceeding with commercialisation.

Conclusions

The GM crops that have been introduced so farand have been, in cases such as herbicide tolerantsoybean, extremely successful will continue to beused by farmers around the world. It is also likelythat the traits that have proved successful will beintroduced into other crop species. Glyphosatetolerance, for example, has been engineered into awide variety of crops from wheat to onions (Eady etal., 2003) and the wheat is already being consideredfor approval for commercial release in NorthAmerica and Australia.

Despite this, the only significant use of GM cropsin the European Union at present is the cultivationof Bt maize in Spain and it is almost inconceivableunder the present circumstances that a companywould develop a GM crop specifically for theEuropean market. Europe might continue to get spin-off products with traits that have been shown to besuccessful elsewhere. However, biotechnologycompanies appear to be focussing more on gainingapproval for the import of GM crop products fromoutside the EU rather than for cultivation within it.This means that European farmers may not be ableto grow GM crops but they will have to competewith them.

Acknowledgement

Rothamsted Research receives grant-aided supportfrom the Biotechnology and Biological SciencesResearch Council of the United Kingdom.

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